- Email: [email protected]
A focused exercise regimen improves clinical measures of balance in patients with peripheral neuropathy
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A Focused Exercise Regimen Improves Clinical Measures of Balance in Patients With Peripheral Neuropathy James K. Richardson, MD, David Sandman, BS, Steve Vela, BS ABSTRACT. Richardson JK, Sandman D, Vela S. A focused exercise regimen improves clinical measures of balance in patients with peripheral neuropathy. Arch Phys Med Rehabil 2001;82:205-9. Objective: To determine the effect of a specific exercise regimen on clinical measures of postural stability and confidence in a population with peripheral neuropathy (PN). Design: Prospective, controlled, single blind study. Setting: Outpatient clinic of a university hospital. Participants: Twenty subjects with diabetes mellitus and electrodiagnostically confirmed PN. Intervention: Ten subjects underwent a 3-week intervention exercise regimen designed to increase rapidly available distal strength and balance. The other 10 subjects performed a control exercise regimen. Main Outcome Measures: Unipedal stance time, functional reach, tandem stance time, and score on the activities-specific balance and confidence (ABC) scale. Results: The intervention subjects, but not the control subjects, showed significant improvement in all 3 clinical measures of balance and nonsignificant improvement on the ABC scale. Conclusion: A brief, specific exercise regimen improved clinical measures of balance in patients with diabetic PN. Further studies are needed to determine if this result translates into a lower fall frequency in this high-risk population. Key Words: Balance; Diabetes mellitus; Exercise; Peripheral nervous system diseases; Rehabilitation. © 2001 by the American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation N PREVIOUS WORK, we found that older persons with neuropathy (PN) are at a markedly increased risk Iforperipheral falls when compared with older persons with healthy pe1,2
ripheral nerves. This postural instability was confirmed in the laboratory setting. Subjects with PN balanced less reliably on 1 foot for 3 seconds than did matched control subjects without PN.3 In addition, a decreased unipedal stance time among persons with PN has, in 2 separate studies, been associated with a history of falls over the previous year.2,4 It has also been noted that diabetic subjects with PN, as identified by decreased
From the Department of Physical Medicine and Rehabilitation (Richardson), University of Michigan (Sandman, Vela), Ann Arbor, MI. Accepted in revised form May 23, 2000. Supported by the University of Michigan Department of Physical Medicine, Public Health Service (grant no. AG-08808), and the University of Michigan Geriatrics Research and Training Center. No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit upon the authors or upon any organization with which the authors are associated. Reprint requests to James K. Richardson, Dept of Physical Medicine and Rehabilitation, 1500 E Medical Center Dr, D5200, University of Michigan Health Systems, Ann Arbor, MI 48109-0718, e-mail: [email protected]. 0003-9993/01/8201-6014$35.00/0 doi:10.1053/apmr.2001.19742
distal vibratory thresholds, were 15 times more likely to report an injury from a fall than a control diabetic group.5 Furthermore, PN is common among older persons, particularly those with diabetes mellitus. Among people over 60 with type 2 diabetes mellitus, the prevalence of PN is greater than 50%.6 Taken together, the data suggest that PN is common among older persons and markedly increases their fall risk. We have identified specific, distal sensory and motor impairments in older persons with PN that appear to underlie their postural instability. The sensory impairments identified are increases in ankle inversion and eversion proprioceptive thresholds, which are about 5 times greater in older persons with PN compared with older persons without PN (1.46° vs 0.3°).7 As a result, older persons with PN are likely less able to perceive ground irregularities and subtle shifts in their centers of mass, and are, therefore, predisposed to falls. More recently, we8 identified a distal motor impairment about the ankle in women who had PN and diabetes. These women showed a significantly decreased ankle rate of torque development compared with the age-matched women with diabetes but no PN (78.2 ⫾ 50.8N 䡠 m/s vs 152.7 ⫾ 54.6N 䡠 m/s, p ⫽ .016). A second outcome was the ability to recover balance on 1 foot when released from a lateral leaning posture (quantified as a percentage of foot width). Three of the 6 women with diabetes but no PN were able to recover from a 5% lean, whereas none of the women with PN was able to recover her balance ( p ⫽ .083). These findings suggest that older women with diabetes and PN have impaired ability to rapidly develop torque at the ankle, which has an impact on balance. It is not known if an exercise regimen will improve the balance impairments identified in older persons with PN. Therefore, our primary hypothesis was that older persons with PN who perform an exercise regimen designed to increase rapidly available ankle strength would show improved balance, as reflected by increased functional reach, as well as tandem and unipedal stance times, compared with those who perform a control exercise regimen. Our secondary hypothesis was that subjects who performed the intervention exercises would show greater confidence, on a validated scale, in their mobility skills (vs the control group). METHODS Subjects The study was approved by the institution’s review board. All subjects gave written and verbal consent. Inclusion criteria included: (1) being between 50 and 80 years old; (2) a known history of diabetes mellitus treated by diet, oral hypoglycemic, or insulin therapy; (3) lower extremity symptoms consistent with PN; (4) ability to walk household distances without assistance or an assistive device (though subjects may use a cane intermittently in the community); (5) willingness to participate in the study; (6) strength of ankle dorsiflexors, invertors, and evertors at least antigravity (grade 3 or greater by manual muscle testing); and (7) conclusive electrodiagnostic evidence of a diffuse, primarily axonal, peripheral polyneuropathy as evidenced by: Arch Phys Med Rehabil Vol 82, February 2001
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(a) sural response: absent or decreased amplitude (⬍6V) with a normal or minimally prolonged distal latency (⬍5ms) stimulating 14cm from the recording site posterior to the lateral malleolus.9 If the sural response was absent bilaterally, the motor responses were not performed. (b) peroneal or tibial responses: absent or decreased in amplitude (⬍2mV for peroneal, ⬍3mV for tibial) with a normal distal latency (⬍6.2ms stimulating 9 and 8cm from recording sites over the extensor digitorum brevis and abductor hallicus muscles, respectively).9 Exclusion criteria included: (1) a history or evidence on physical examination of significant central nervous system dysfunction (ie, hemiparesis, myelopathy, cerebellar ataxia); (2) significant musculoskeletal deformity (ie, amputation, scoliosis, abnormality of range of motion [ROM]) that would prevent participation (⬍90° of humeral abduction, inability to grip, ⬍10° of combined ankle inversion/eversion); (3) lower extremity arthritis or pain that limits standing or weight-bearing exercise; (4) electrodiagnostic evidence of any diagnosis other than PN; (5) a history or evidence on physical examination of vestibular dysfunction; (6) a history of angina or anginaequivalent symptoms (ie, nausea, diaphoresis, shortness of breath with exercise); (7) symptomatic postural hypotension (postural lightheadedness that interferes with standing for 5min); and (8) a history or evidence on physical examination of plantar skin pressure ulcer. The subjects also were evaluated by using the Michigan Diabetes Neuropathy Score (MDNS).10 This is a 46-point scale (0 – 46, with higher score reflecting more severe PN) that has been shown to correlate well with more extensive neuropathy staging scales. The scale includes muscle stretch reflexes at the biceps, triceps, patella, and Achilles; pinprick sensation at the great toe; ability to perceive the touch of a 10-gram monofilament; ability to perceive a 128Hz tuning fork at the great toe; strength of hand dorsal interossei; great toe extension; and ankle dorsiflexion. The first 10 subjects recruited were placed in the intervention group, and the next 10 subjects were placed in the control group. Intervention Exercises The exercise interventions, performed daily on a firm surface for 3 weeks, included: (1) Warm up (open chain active ankle ROM exercises). Subjects wrote the alphabet in the air with each foot by moving the ankle. (2) Bipedal toe raises and heel raises (lifting the forefoot as one does to balance on a heel). Subjects did these as quickly as possible, using support as necessary. Subjects started with 1 set of 10 and increased by 1 set every 5 exercise sessions for a total of 3 sets. (3) Bipedal inversion and eversion. In this exercise, subjects’ center of mass was shifted laterally as subjects strengthened ankle invertors and evertors via closed chain exercises. The goal was to do so without using the upper extremities, but support was used as necessary. Subjects started with 10 repetitions in each direction and increased to 2 sets of 10 repetitions after 5 exercise sessions. (4) Unipedal toe raises and heel raises. Again, subjects attempted to perform this quickly— even if that was not possible. Subjects started with 5 repetitions of each exercise and increased to 10 repetitions after 5 exercises and then to 2 sets of 10 after 10 exercise sessions. (5) Unipedal inversion and eversion. Subjects inverted and everted the foot while standing on it to challenge balance Arch Phys Med Rehabil Vol 82, February 2001
and to create a closed chain exercise of the ankle invertors and evertors. It was anticipated that most subjects would find this task challenging and so they used their hands for balance when needed. Subjects started with 1 set of 5 repetitions in each direction and increased to 10 repetitions after 5 exercise sessions. (6) Wall slides. Subjects started with bipedal slides with knee flexion maximum of about 45°. They performed 3 sets of 10. After 5 exercise sessions the first set was performed on each foot. (7) Unipedal balance for time. Three tries on each foot. Control Exercises The control exercise regimen was performed in a seated position. Subjects performed neck flexion and rotation stretching with eyes open and then closed. They then used a resistance band to perform strengthening exercises for the scapular abductors, shoulder external rotators, and elbow flexors. The exercises were performed 5 or more times (if tolerated) per week for 3 weeks. Control exercises were suggested at a slightly decreased frequency because of concern that they might lead to an overuse injury, which was not felt to be an ethical risk from a control intervention. Outcomes All subjects underwent 3 trials of tandem stance, functional reach, and unipedal stance before and after their exercise programs. Tandem stance, functional reach, and unipedal stance were performed and graded as described elsewhere.2,11,12 In addition, all subjects filled out the activitiesspecific balance confidence (ABC) scale13 before and after the exercise regimen. The ABC scale lists 16 activities (eg, walking up and down stairs, walking on an icy sidewalk) and subjects describe their degree of confidence in performing each activity, on a scale from 0% (no confidence) to 100% (complete confidence). All subjects were evaluated before and after their 3-week exercise programs by the same examiner (DS). Statistical Analysis A paired, 2-tailed t test was used to detect significant changes in tandem stance, functional reach, and unipedal stance. A p value of less than .05 was considered significant and a p value of .05 or greater and less than .10 was considered a trend. A 2-tailed t test was also used for evaluating the responses to the 16 activities on the ABC scale; however, to compensate for making multiple comparisons, p less than .0125 was considered significant and p .125 or greater and less than .025 was considered a trend. RESULTS Nine of the 10 intervention subjects and 7 of the 10 control subjects completed the study. The intervention subject dropped out because of foot-ankle pain, which was attributed to the exercise regimen aggravating an underlying arthritis. One of the 3 control subjects developed an illness and 2 dropped out without specifying a reason. Subject characteristics of gender and age are listed in table 1. There was a trend toward an increased MDNS score, representing more severe PN, among the intervention subjects compared with the control subjects (table 1). There was no significant difference between intervention and control subjects’ sural, peroneal motor, or tibial motor response amplitudes. The 2 groups showed grossly similar baseline values for tandem stance and functional reach. The shorter unipedal stance time at baseline in the intervention group, compared
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NEUROPATHY, BALANCE, AND EXERCISE, Richardson Table 1: Clinical Characteristics of Subjects
Age (yr) (mean ⫾ SD) Gender (% men) MDNS score (⫾SD)* Response amplitudes Sural (V) Peroneal motor (mV) Tibial motor (mV)
Intervention Group (n ⫽ 9)
Control Group (n ⫽ 7)
p
64.0 ⫾ 6.3 8 (89%) 18.6 ⫾ 5.3
63.3 ⫾ 7.6 4 (57%) 11.9 ⫾ 3.0
NS NS .060†
.25 ⫾ .79 .57 ⫾ .63 .18 ⫾ .33
.15 ⫾ .47 .33 ⫾ .43 .50 ⫾ 1.1
.34 .11 .27
Abbreviation: NS, not significant. * MDNS scores: higher score ⫽ more severe neuropathy (maximum ⫽ 46). † Represents a trend toward more severe neuropathy in the intervention group versus the control group.
with the control group ( p ⫽ .11), was consistent with the trend toward an increased MDNS score in the intervention group; however, none of the baseline differences was significant. The intervention subjects showed a significant improvement in all 3 outcomes after the exercise regimen (table 2). In contrast, the control subjects showed insignificant improvements in tandem stance and functional reach, and an insignificant decrease in unipedal stance time (table 2). The intervention and control groups showed nearly identical initial composite confidence scores (table 3). Although the intervention group reported improved confidence, as reflected by a greater composite ABC score postintervention, the difference was not significant. There was no significant change in the control group confidence scores. When confidence scores for isolated activities were considered, there was a trend toward the intervention subjects reporting greater confidence in climbing and descending stairs after the intervention exercises (table 3). The intervention group also reported a 10% or greater improvement in confidence for 3 other activities (bending over to pick up an object, standing on tip toes to reach overhead, walking on icy sidewalks), but the changes were not significant. The control group showed no significant changes or trends toward a change after their exercise program. There was a change of 10% toward greater confidence among the control group for bending over to pick up an object. DISCUSSION The data from this study showed that an exercise regimen designed to increase rapidly available ankle strength improved 3 commonly used clinical measures of balance (functional reach, tandem stance, unipedal stance) among older persons with mild to moderate PN. The study further showed that these improvements develop in a relatively short period of time and that the exercise regimen is well tolerated. The data also suggested, but did not confirm, that the exercise regimen is associated with improvements in subjects’ confidence in their abilities to perform daily tasks that challenge balance. There was evidence to suggest that exercise is a reasonable intervention, even in those with predominantly sensory PN. Aside from our study, which showed impaired ankle rate of torque development among subjects with clinically normal ankle strength,8 other work suggests that patients with clinically mild or sensory-only PN likely have motor impairments about the ankle. In an electrophysiologic study14 of subjects selected for clinical evidence of sensory-only PN, most subjects (70%) had abnormalities during needle electromyography of the anterior tibialis or medial gastrocnemius muscles, both of which provide torque to the ankle. Those investigators14
concluded that “subclinical motor involvement is often detected on electrophysiologic studies in patients . . . who have only sensory signs.” Also, there is evidence in animal models15 and in humans16 that the number of type II muscle fibers not only decreases with age, but that there is a preferential loss of type II motor units in the setting of denervation, particularly distal denervation.17 Therefore, it appears likely that a generalized PN, even among patients with predominantly sensory findings, is associated with motor deficits characterized by decreased rapidly available torque at the ankle. This impairment, though important for postural stability under challenging circumstances, is likely difficult or impossible to detect on routine physical examination and, therefore, remains subclinical. Because functional reach and tandem stance were not part of the intervention exercise regimen, improvement in these outcomes suggests that some change occurred beyond a practice effect. It is possible that the intervention subjects increased their ankle strength in response to the exercise regimen. Brown et al18 found that type II muscle fiber concentration significantly increased in older persons undergoing rigorous strengthening programs. The intervention applied in our study was designed to increase rapidly available torque about the ankle19 and recruit type II motor units.20 Brown18 tested the biceps, a proximal upper extremity muscle, and, therefore, their findings may not apply to distal lower extremity muscles, which were the target of strengthening in our study. Another mechanism of strengthening is possible. Early strength gains appear to be related to neural changes—possibly improved synchronization of motor units—rather than muscle hypertrophy.21 Strengthening has, therefore, been found to occur in response to exercise in diseases such as hereditary motor and sensory neuropathy types I and II22 and postpoliomyelitis syndrome,23 which decrease available motor units in a manner similar to that of a generalized PN. Given the brevity of the exercise intervention, any strengthening that occurred in the intervention group was more likely related to a synchronization of motor units rather than muscle hypertrophy. An isolated improvement in the strength of the ankle musculature would likely be sufficient to lead to the improvements noted in this study. Others have found that increased muscle strength among older subjects was an independent predictor of a decreased risk for loss of balance during a difficult test of balance that reduced proprioceptive input, a condition that mimics the patient with PN.24 Wolfson et al25 emphasized the strong association between falls/loss of balance and decreased ankle strength among nursing home residents. However, an improvement in ankle muscle strength, and, therefore, muscle tension, may also improve ankle proprioceptive thresholds. In
Table 2: Change in Clinical Measures of Balance Pre- and Postexercise
Intervention Group Tandem stance (s) Functional reach (in) Unipedal stance (s) Control Group Tandem stance (s) Functional reach (in) Unipedal stance (s)
Preexercise
Postexercise
p*
17.5 ⫾ 13.4 10.5 ⫾ 2.1 5.4 ⫾ 4.7
23.5 ⫾ 10.9 11.5 ⫾ 2.2 11.6 ⫾ 10.2
.004 .0012 .0014
19.0 ⫾ 11.8 11.3 ⫾ 3.6 9.3 ⫾ 8.6
22.0 ⫾ 12.0 11.9 ⫾ 2.8 7.9 ⫾ 5.9
.13 .23 .33
NOTE. Values presented as mean ⫾ SD. * Two-tailed t test.
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NEUROPATHY, BALANCE, AND EXERCISE, Richardson Table 3: Change in Subject Responses on the ABC Scale Intervention Group
Question 2* Question 3 Question 5 Question 16 Mean of all questions
Control Group
Before
After
p
Before
After
p
70 ⫾ 28 81 ⫾ 24 78 ⫾ 26 51 ⫾ 38 80 ⫾ 21
83 ⫾ 16 93 ⫾ 9 90 ⫾ 13 67 ⫾ 32 88 ⫾ 11
.022† .093 .093 .048 .14
76 ⫾ 14 76 ⫾ 29 77 ⫾ 30 60 ⫾ 36 80 ⫾ 21
81 ⫾ 21 86 ⫾ 18 76 ⫾ 28 62 ⫾ 32 80 ⫾ 20
.36 .11 .36 .45 .64
NOTE. Values presented as %, in mean ⫾ SD. * 100% ⫽ complete confidence for activity; 0% ⫽ no confidence for activity. See text for activities. † Represents a trend toward intervention subjects reporting greater confidence after the exercise regimen.
another study, perception of ankle plantar- and dorsiflexion improved markedly when the calf musculature was tested under tension compared with when the musculature was relaxed.26 Among the present study’s strengths is the careful subject selection, using electrodiagnostic criteria to confirm the presence of PN, and the use of a control group with a control exercise regimen. In addition, the outcomes are thought to have clinical meaning; impairments in 2 of the 3 outcomes— unipedal stance and functional reach— have been associated with injurious falls.12,27 Our study was well controlled, with the control subjects receiving attention equivalent to the intervention group. In addition, the control subjects showed their greatest improvement on the ABC scale for a task involving gross head motion, similar to some of their exercises, suggesting the possibility that those subjects found the control exercises meaningful. Our study’s greatest limitation was its design: it was not double-blind. Although the tests were administered as objectively as possible, bias is possible. This seems less likely for unipedal stance, which requires little judgment on the examiner’s part. The decreased MDNS score and increased unipedal stance time of the control subjects1 preexercise suggests that they had less severe PN than the intervention subjects. However, the control subjects still had much room to improve— particularly in tandem and unipedal stance—so that a ceiling effect does not appear to be an explanation for their lack of improvement. Although the subjects were carefully selected and had similar baseline characteristics, the relatively small numbers diminish the strength of the conclusions. A larger study is planned to confirm the findings of our work. A last concern is that most subjects were men. Therefore, translating these results to women should be performed with caution. CONCLUSION A brief, intense exercise regimen designed to improve distal lower extremity strength was well tolerated and improved 3 clinical parameters of balance in a group of older persons with PN. Although increased confidence or distal lower extremity strength may be responsible for these findings, the study provided no clear insight into the mechanism of the improvements seen in the intervention group. Whether the improvements in clinical balance noted in the intervention subjects translate into decreased fall risk in daily life is unknown. However, given the minimal risk from the intervention exercises and the magnitude of the benefit from preventing falls in the population studied, it appears reasonable for clinicians to consider prescribing these exercises for their patients with postural instability caused by PN. Arch Phys Med Rehabil Vol 82, February 2001
References 1. Richardson JK, Ching C, Hurvitz EA. The relationship between electromyographically documented peripheral neuropathy and falls. J Am Geriatr Soc 1992;40:1008-12. 2. Richardson JK, Hurvitz EA. Peripheral neuropathy: a true risk factor for falls. J Gerontol A Biol Sci Med Sci 1995;50:M211-5. 3. Richardson JK, Ashton-Miller JA, Lee SG, Jacobs K. Moderate peripheral neuropathy impairs weight transfer and unipedal balance in the elderly. Arch Phys Med Rehabil 1996;77:1152-6. 4. Hurvitz EA, Richardson JK, Werner RA, Ruhl A, Dixon M. Unipedal stance testing as an indicator of fall risk among older outpatients. Arch Phys Med Rehabil 2000;81:587-91. 5. Cavanagh PR, Derr JA, Ulbrecht JS, Maser RE, Orchard TJ. Problems with gait and posture in neuropathic patients with insulin-dependent diabetes mellitus. Diabetic Med 1992;9:469-74. 6. Young M, Boultin A, Maclead A, Williams D, Sonksen P. A multicentre study of the prevalence of diabetic peripheral neuropathy in the United Kingdom hospital clinic population. Diabetologia 1993;36:150-4. 7. Van de Bosh C, Gilsing MG, Lee SG, Richardson JK, AshtonMiller JA. Peripheral neuropathy effect on ankle inversion and eversion thresholds. Arch Phys Med Rehabil 1995;76:850-6. 8. Gutierrez MS, Helber MB, Dealva D, Ashton-Miller, Richardson JK. Mild diabetic neuropathy affects ankle motor function. Diabetes Care. In press. 9. Liveson JA, Ma DM, editors. Laboratory reference for clinical neurophysiology. Philadelphia: FA Davis; 1992. 10. Feldman EL, Stevens MJ, Thomas PK, Brown MB, Canal N, Greene DA. A practical two-step quantitative clinical and eletrophysiological assessment for the diagnosis and staging of diabetic neuropathy. Diabetes Care 1994;17:1281-9. 11. Berg KO, Wood-Dauphinee SL, Williams JI, Maki B. Measuring balance in the elderly: validation of an instrument. Can J Public Health 1992;83(Suppl 2):S7-11. 12. Duncan PW, Studenski S, Chandler J, Prescott B. Functional reach: predictive validity in a sample of elderly male veterans. J Gerontol A Biol Sci Med Sci 1992;47:M93-8. 13. Powell LE, Myers AM. The activities-specific balance confidence (ABC) scale. J Gerontol A Biol Sci Med Sci 1995;50:M28-34. 14. Bril V, Werb MR, Greene DA, Sima AAF. Single-fiber electromyography in diabetic peripheral polyneuropathy. Muscle Nerve 1996;19:2-9. 15. Kadhiresan VA, Hassett CA, Faulkner JA. Properties of single motor units in medial gastrocnemius muscles of adult and old rats. J Physiol 1996;493(Pt 2):43-52. 16. Hakkinen K, Kraemer WJ, Kallinen M, Linnamo V, Pastinem UM, Newton RU. Bilateral and unilateral neuromuscular function and muscle cross-sectional area in middle-aged and elderly men and women. J Gerontol A Biol Sci Med Sci 1996;51:21-9. 17. Bishop DL, Milton RL. The effects of denervation location on fiber type mix in self-reinnervated mouse soleus muscles. Exp Neurol 1997;147:151-8. 18. Brown AB, McCartney N, Sale DG. Positive adaptations to weight-lifting training in the elderly. J Appl Physiol 1990;69: 1725-33.
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19. Behm DG, Sale DG. Intended rather than actual movement velocity determines velocity specific training response. J Appl Physiol 1993;74:359-68. 20. Vandervoort AA, Sale DG, Moroz J. Comparison of motor unit activation during unilateral and bilateral leg extension. J Appl Physiol 1984;56:46-51. 21. Moritani T, de Vries HA. Neural factors versus hypertrophy in the time course of muscle strength gain. Am J Phys Med 1979;58: 115-30. 22. Lindeman E, Leffers P, Spaans F, Drukker J, Reulen J, Ierchkoffs M, et al. Strength training in patients with myotonic dystrohy and hereditary motor and sensory neuropathy: a randomized clinical trial. Arch Phys Med Rehabil 1995;76:612-20. 23. Agre JC, Rodriguez AA, Harmon RL, Swiggum ER, Franke TM. Strengthening exercise can improve muscle function in post-polio
24. 25. 26. 27.
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subjects without detectable adverse effect upon the surviving motor units or muscle [abstract]. Arch Phys Med Rehabil 1995; 76:1036. Judge JO, King MB, Whipple R, Clive J, Wolfson LI. Dynamic balance in older persons: effects of reduced visual and proprioceptive input. J Gerontol A Biol Sci Med Sci 1995;50:M263-70. Wolfson L, Judge J, Whipple R, King M. Strength is a major factor in balance, gait, and the occurrence of falls. J Gerontol A Biol Sci Med Sci 1995;50:64-7. Refshauge KM, Fitzpatrick RC. Perception of movement at the human ankle: effects of leg position. J Physiol 1995;488(Pt 1): 243-8. Vellas BJ, Wayne SJ, Romero L, Baumgartner RN, Rubenstein LZ, Garry PJ. One-leg balance is an important predictor of injurious falls in older persons. J Am Geriatr Soc 1997;45:735-8.
Arch Phys Med Rehabil Vol 82, February 2001
A Focused Exercise Regimen Improves Clinical Measures of Balance in Patients With Peripheral Neuropathy James K. Richardson, MD, David Sandman, BS, Steve Vela, BS ABSTRACT. Richardson JK, Sandman D, Vela S. A focused exercise regimen improves clinical measures of balance in patients with peripheral neuropathy. Arch Phys Med Rehabil 2001;82:205-9. Objective: To determine the effect of a specific exercise regimen on clinical measures of postural stability and confidence in a population with peripheral neuropathy (PN). Design: Prospective, controlled, single blind study. Setting: Outpatient clinic of a university hospital. Participants: Twenty subjects with diabetes mellitus and electrodiagnostically confirmed PN. Intervention: Ten subjects underwent a 3-week intervention exercise regimen designed to increase rapidly available distal strength and balance. The other 10 subjects performed a control exercise regimen. Main Outcome Measures: Unipedal stance time, functional reach, tandem stance time, and score on the activities-specific balance and confidence (ABC) scale. Results: The intervention subjects, but not the control subjects, showed significant improvement in all 3 clinical measures of balance and nonsignificant improvement on the ABC scale. Conclusion: A brief, specific exercise regimen improved clinical measures of balance in patients with diabetic PN. Further studies are needed to determine if this result translates into a lower fall frequency in this high-risk population. Key Words: Balance; Diabetes mellitus; Exercise; Peripheral nervous system diseases; Rehabilitation. © 2001 by the American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation N PREVIOUS WORK, we found that older persons with neuropathy (PN) are at a markedly increased risk Iforperipheral falls when compared with older persons with healthy pe1,2
ripheral nerves. This postural instability was confirmed in the laboratory setting. Subjects with PN balanced less reliably on 1 foot for 3 seconds than did matched control subjects without PN.3 In addition, a decreased unipedal stance time among persons with PN has, in 2 separate studies, been associated with a history of falls over the previous year.2,4 It has also been noted that diabetic subjects with PN, as identified by decreased
From the Department of Physical Medicine and Rehabilitation (Richardson), University of Michigan (Sandman, Vela), Ann Arbor, MI. Accepted in revised form May 23, 2000. Supported by the University of Michigan Department of Physical Medicine, Public Health Service (grant no. AG-08808), and the University of Michigan Geriatrics Research and Training Center. No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit upon the authors or upon any organization with which the authors are associated. Reprint requests to James K. Richardson, Dept of Physical Medicine and Rehabilitation, 1500 E Medical Center Dr, D5200, University of Michigan Health Systems, Ann Arbor, MI 48109-0718, e-mail: [email protected]. 0003-9993/01/8201-6014$35.00/0 doi:10.1053/apmr.2001.19742
distal vibratory thresholds, were 15 times more likely to report an injury from a fall than a control diabetic group.5 Furthermore, PN is common among older persons, particularly those with diabetes mellitus. Among people over 60 with type 2 diabetes mellitus, the prevalence of PN is greater than 50%.6 Taken together, the data suggest that PN is common among older persons and markedly increases their fall risk. We have identified specific, distal sensory and motor impairments in older persons with PN that appear to underlie their postural instability. The sensory impairments identified are increases in ankle inversion and eversion proprioceptive thresholds, which are about 5 times greater in older persons with PN compared with older persons without PN (1.46° vs 0.3°).7 As a result, older persons with PN are likely less able to perceive ground irregularities and subtle shifts in their centers of mass, and are, therefore, predisposed to falls. More recently, we8 identified a distal motor impairment about the ankle in women who had PN and diabetes. These women showed a significantly decreased ankle rate of torque development compared with the age-matched women with diabetes but no PN (78.2 ⫾ 50.8N 䡠 m/s vs 152.7 ⫾ 54.6N 䡠 m/s, p ⫽ .016). A second outcome was the ability to recover balance on 1 foot when released from a lateral leaning posture (quantified as a percentage of foot width). Three of the 6 women with diabetes but no PN were able to recover from a 5% lean, whereas none of the women with PN was able to recover her balance ( p ⫽ .083). These findings suggest that older women with diabetes and PN have impaired ability to rapidly develop torque at the ankle, which has an impact on balance. It is not known if an exercise regimen will improve the balance impairments identified in older persons with PN. Therefore, our primary hypothesis was that older persons with PN who perform an exercise regimen designed to increase rapidly available ankle strength would show improved balance, as reflected by increased functional reach, as well as tandem and unipedal stance times, compared with those who perform a control exercise regimen. Our secondary hypothesis was that subjects who performed the intervention exercises would show greater confidence, on a validated scale, in their mobility skills (vs the control group). METHODS Subjects The study was approved by the institution’s review board. All subjects gave written and verbal consent. Inclusion criteria included: (1) being between 50 and 80 years old; (2) a known history of diabetes mellitus treated by diet, oral hypoglycemic, or insulin therapy; (3) lower extremity symptoms consistent with PN; (4) ability to walk household distances without assistance or an assistive device (though subjects may use a cane intermittently in the community); (5) willingness to participate in the study; (6) strength of ankle dorsiflexors, invertors, and evertors at least antigravity (grade 3 or greater by manual muscle testing); and (7) conclusive electrodiagnostic evidence of a diffuse, primarily axonal, peripheral polyneuropathy as evidenced by: Arch Phys Med Rehabil Vol 82, February 2001
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(a) sural response: absent or decreased amplitude (⬍6V) with a normal or minimally prolonged distal latency (⬍5ms) stimulating 14cm from the recording site posterior to the lateral malleolus.9 If the sural response was absent bilaterally, the motor responses were not performed. (b) peroneal or tibial responses: absent or decreased in amplitude (⬍2mV for peroneal, ⬍3mV for tibial) with a normal distal latency (⬍6.2ms stimulating 9 and 8cm from recording sites over the extensor digitorum brevis and abductor hallicus muscles, respectively).9 Exclusion criteria included: (1) a history or evidence on physical examination of significant central nervous system dysfunction (ie, hemiparesis, myelopathy, cerebellar ataxia); (2) significant musculoskeletal deformity (ie, amputation, scoliosis, abnormality of range of motion [ROM]) that would prevent participation (⬍90° of humeral abduction, inability to grip, ⬍10° of combined ankle inversion/eversion); (3) lower extremity arthritis or pain that limits standing or weight-bearing exercise; (4) electrodiagnostic evidence of any diagnosis other than PN; (5) a history or evidence on physical examination of vestibular dysfunction; (6) a history of angina or anginaequivalent symptoms (ie, nausea, diaphoresis, shortness of breath with exercise); (7) symptomatic postural hypotension (postural lightheadedness that interferes with standing for 5min); and (8) a history or evidence on physical examination of plantar skin pressure ulcer. The subjects also were evaluated by using the Michigan Diabetes Neuropathy Score (MDNS).10 This is a 46-point scale (0 – 46, with higher score reflecting more severe PN) that has been shown to correlate well with more extensive neuropathy staging scales. The scale includes muscle stretch reflexes at the biceps, triceps, patella, and Achilles; pinprick sensation at the great toe; ability to perceive the touch of a 10-gram monofilament; ability to perceive a 128Hz tuning fork at the great toe; strength of hand dorsal interossei; great toe extension; and ankle dorsiflexion. The first 10 subjects recruited were placed in the intervention group, and the next 10 subjects were placed in the control group. Intervention Exercises The exercise interventions, performed daily on a firm surface for 3 weeks, included: (1) Warm up (open chain active ankle ROM exercises). Subjects wrote the alphabet in the air with each foot by moving the ankle. (2) Bipedal toe raises and heel raises (lifting the forefoot as one does to balance on a heel). Subjects did these as quickly as possible, using support as necessary. Subjects started with 1 set of 10 and increased by 1 set every 5 exercise sessions for a total of 3 sets. (3) Bipedal inversion and eversion. In this exercise, subjects’ center of mass was shifted laterally as subjects strengthened ankle invertors and evertors via closed chain exercises. The goal was to do so without using the upper extremities, but support was used as necessary. Subjects started with 10 repetitions in each direction and increased to 2 sets of 10 repetitions after 5 exercise sessions. (4) Unipedal toe raises and heel raises. Again, subjects attempted to perform this quickly— even if that was not possible. Subjects started with 5 repetitions of each exercise and increased to 10 repetitions after 5 exercises and then to 2 sets of 10 after 10 exercise sessions. (5) Unipedal inversion and eversion. Subjects inverted and everted the foot while standing on it to challenge balance Arch Phys Med Rehabil Vol 82, February 2001
and to create a closed chain exercise of the ankle invertors and evertors. It was anticipated that most subjects would find this task challenging and so they used their hands for balance when needed. Subjects started with 1 set of 5 repetitions in each direction and increased to 10 repetitions after 5 exercise sessions. (6) Wall slides. Subjects started with bipedal slides with knee flexion maximum of about 45°. They performed 3 sets of 10. After 5 exercise sessions the first set was performed on each foot. (7) Unipedal balance for time. Three tries on each foot. Control Exercises The control exercise regimen was performed in a seated position. Subjects performed neck flexion and rotation stretching with eyes open and then closed. They then used a resistance band to perform strengthening exercises for the scapular abductors, shoulder external rotators, and elbow flexors. The exercises were performed 5 or more times (if tolerated) per week for 3 weeks. Control exercises were suggested at a slightly decreased frequency because of concern that they might lead to an overuse injury, which was not felt to be an ethical risk from a control intervention. Outcomes All subjects underwent 3 trials of tandem stance, functional reach, and unipedal stance before and after their exercise programs. Tandem stance, functional reach, and unipedal stance were performed and graded as described elsewhere.2,11,12 In addition, all subjects filled out the activitiesspecific balance confidence (ABC) scale13 before and after the exercise regimen. The ABC scale lists 16 activities (eg, walking up and down stairs, walking on an icy sidewalk) and subjects describe their degree of confidence in performing each activity, on a scale from 0% (no confidence) to 100% (complete confidence). All subjects were evaluated before and after their 3-week exercise programs by the same examiner (DS). Statistical Analysis A paired, 2-tailed t test was used to detect significant changes in tandem stance, functional reach, and unipedal stance. A p value of less than .05 was considered significant and a p value of .05 or greater and less than .10 was considered a trend. A 2-tailed t test was also used for evaluating the responses to the 16 activities on the ABC scale; however, to compensate for making multiple comparisons, p less than .0125 was considered significant and p .125 or greater and less than .025 was considered a trend. RESULTS Nine of the 10 intervention subjects and 7 of the 10 control subjects completed the study. The intervention subject dropped out because of foot-ankle pain, which was attributed to the exercise regimen aggravating an underlying arthritis. One of the 3 control subjects developed an illness and 2 dropped out without specifying a reason. Subject characteristics of gender and age are listed in table 1. There was a trend toward an increased MDNS score, representing more severe PN, among the intervention subjects compared with the control subjects (table 1). There was no significant difference between intervention and control subjects’ sural, peroneal motor, or tibial motor response amplitudes. The 2 groups showed grossly similar baseline values for tandem stance and functional reach. The shorter unipedal stance time at baseline in the intervention group, compared
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NEUROPATHY, BALANCE, AND EXERCISE, Richardson Table 1: Clinical Characteristics of Subjects
Age (yr) (mean ⫾ SD) Gender (% men) MDNS score (⫾SD)* Response amplitudes Sural (V) Peroneal motor (mV) Tibial motor (mV)
Intervention Group (n ⫽ 9)
Control Group (n ⫽ 7)
p
64.0 ⫾ 6.3 8 (89%) 18.6 ⫾ 5.3
63.3 ⫾ 7.6 4 (57%) 11.9 ⫾ 3.0
NS NS .060†
.25 ⫾ .79 .57 ⫾ .63 .18 ⫾ .33
.15 ⫾ .47 .33 ⫾ .43 .50 ⫾ 1.1
.34 .11 .27
Abbreviation: NS, not significant. * MDNS scores: higher score ⫽ more severe neuropathy (maximum ⫽ 46). † Represents a trend toward more severe neuropathy in the intervention group versus the control group.
with the control group ( p ⫽ .11), was consistent with the trend toward an increased MDNS score in the intervention group; however, none of the baseline differences was significant. The intervention subjects showed a significant improvement in all 3 outcomes after the exercise regimen (table 2). In contrast, the control subjects showed insignificant improvements in tandem stance and functional reach, and an insignificant decrease in unipedal stance time (table 2). The intervention and control groups showed nearly identical initial composite confidence scores (table 3). Although the intervention group reported improved confidence, as reflected by a greater composite ABC score postintervention, the difference was not significant. There was no significant change in the control group confidence scores. When confidence scores for isolated activities were considered, there was a trend toward the intervention subjects reporting greater confidence in climbing and descending stairs after the intervention exercises (table 3). The intervention group also reported a 10% or greater improvement in confidence for 3 other activities (bending over to pick up an object, standing on tip toes to reach overhead, walking on icy sidewalks), but the changes were not significant. The control group showed no significant changes or trends toward a change after their exercise program. There was a change of 10% toward greater confidence among the control group for bending over to pick up an object. DISCUSSION The data from this study showed that an exercise regimen designed to increase rapidly available ankle strength improved 3 commonly used clinical measures of balance (functional reach, tandem stance, unipedal stance) among older persons with mild to moderate PN. The study further showed that these improvements develop in a relatively short period of time and that the exercise regimen is well tolerated. The data also suggested, but did not confirm, that the exercise regimen is associated with improvements in subjects’ confidence in their abilities to perform daily tasks that challenge balance. There was evidence to suggest that exercise is a reasonable intervention, even in those with predominantly sensory PN. Aside from our study, which showed impaired ankle rate of torque development among subjects with clinically normal ankle strength,8 other work suggests that patients with clinically mild or sensory-only PN likely have motor impairments about the ankle. In an electrophysiologic study14 of subjects selected for clinical evidence of sensory-only PN, most subjects (70%) had abnormalities during needle electromyography of the anterior tibialis or medial gastrocnemius muscles, both of which provide torque to the ankle. Those investigators14
concluded that “subclinical motor involvement is often detected on electrophysiologic studies in patients . . . who have only sensory signs.” Also, there is evidence in animal models15 and in humans16 that the number of type II muscle fibers not only decreases with age, but that there is a preferential loss of type II motor units in the setting of denervation, particularly distal denervation.17 Therefore, it appears likely that a generalized PN, even among patients with predominantly sensory findings, is associated with motor deficits characterized by decreased rapidly available torque at the ankle. This impairment, though important for postural stability under challenging circumstances, is likely difficult or impossible to detect on routine physical examination and, therefore, remains subclinical. Because functional reach and tandem stance were not part of the intervention exercise regimen, improvement in these outcomes suggests that some change occurred beyond a practice effect. It is possible that the intervention subjects increased their ankle strength in response to the exercise regimen. Brown et al18 found that type II muscle fiber concentration significantly increased in older persons undergoing rigorous strengthening programs. The intervention applied in our study was designed to increase rapidly available torque about the ankle19 and recruit type II motor units.20 Brown18 tested the biceps, a proximal upper extremity muscle, and, therefore, their findings may not apply to distal lower extremity muscles, which were the target of strengthening in our study. Another mechanism of strengthening is possible. Early strength gains appear to be related to neural changes—possibly improved synchronization of motor units—rather than muscle hypertrophy.21 Strengthening has, therefore, been found to occur in response to exercise in diseases such as hereditary motor and sensory neuropathy types I and II22 and postpoliomyelitis syndrome,23 which decrease available motor units in a manner similar to that of a generalized PN. Given the brevity of the exercise intervention, any strengthening that occurred in the intervention group was more likely related to a synchronization of motor units rather than muscle hypertrophy. An isolated improvement in the strength of the ankle musculature would likely be sufficient to lead to the improvements noted in this study. Others have found that increased muscle strength among older subjects was an independent predictor of a decreased risk for loss of balance during a difficult test of balance that reduced proprioceptive input, a condition that mimics the patient with PN.24 Wolfson et al25 emphasized the strong association between falls/loss of balance and decreased ankle strength among nursing home residents. However, an improvement in ankle muscle strength, and, therefore, muscle tension, may also improve ankle proprioceptive thresholds. In
Table 2: Change in Clinical Measures of Balance Pre- and Postexercise
Intervention Group Tandem stance (s) Functional reach (in) Unipedal stance (s) Control Group Tandem stance (s) Functional reach (in) Unipedal stance (s)
Preexercise
Postexercise
p*
17.5 ⫾ 13.4 10.5 ⫾ 2.1 5.4 ⫾ 4.7
23.5 ⫾ 10.9 11.5 ⫾ 2.2 11.6 ⫾ 10.2
.004 .0012 .0014
19.0 ⫾ 11.8 11.3 ⫾ 3.6 9.3 ⫾ 8.6
22.0 ⫾ 12.0 11.9 ⫾ 2.8 7.9 ⫾ 5.9
.13 .23 .33
NOTE. Values presented as mean ⫾ SD. * Two-tailed t test.
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NEUROPATHY, BALANCE, AND EXERCISE, Richardson Table 3: Change in Subject Responses on the ABC Scale Intervention Group
Question 2* Question 3 Question 5 Question 16 Mean of all questions
Control Group
Before
After
p
Before
After
p
70 ⫾ 28 81 ⫾ 24 78 ⫾ 26 51 ⫾ 38 80 ⫾ 21
83 ⫾ 16 93 ⫾ 9 90 ⫾ 13 67 ⫾ 32 88 ⫾ 11
.022† .093 .093 .048 .14
76 ⫾ 14 76 ⫾ 29 77 ⫾ 30 60 ⫾ 36 80 ⫾ 21
81 ⫾ 21 86 ⫾ 18 76 ⫾ 28 62 ⫾ 32 80 ⫾ 20
.36 .11 .36 .45 .64
NOTE. Values presented as %, in mean ⫾ SD. * 100% ⫽ complete confidence for activity; 0% ⫽ no confidence for activity. See text for activities. † Represents a trend toward intervention subjects reporting greater confidence after the exercise regimen.
another study, perception of ankle plantar- and dorsiflexion improved markedly when the calf musculature was tested under tension compared with when the musculature was relaxed.26 Among the present study’s strengths is the careful subject selection, using electrodiagnostic criteria to confirm the presence of PN, and the use of a control group with a control exercise regimen. In addition, the outcomes are thought to have clinical meaning; impairments in 2 of the 3 outcomes— unipedal stance and functional reach— have been associated with injurious falls.12,27 Our study was well controlled, with the control subjects receiving attention equivalent to the intervention group. In addition, the control subjects showed their greatest improvement on the ABC scale for a task involving gross head motion, similar to some of their exercises, suggesting the possibility that those subjects found the control exercises meaningful. Our study’s greatest limitation was its design: it was not double-blind. Although the tests were administered as objectively as possible, bias is possible. This seems less likely for unipedal stance, which requires little judgment on the examiner’s part. The decreased MDNS score and increased unipedal stance time of the control subjects1 preexercise suggests that they had less severe PN than the intervention subjects. However, the control subjects still had much room to improve— particularly in tandem and unipedal stance—so that a ceiling effect does not appear to be an explanation for their lack of improvement. Although the subjects were carefully selected and had similar baseline characteristics, the relatively small numbers diminish the strength of the conclusions. A larger study is planned to confirm the findings of our work. A last concern is that most subjects were men. Therefore, translating these results to women should be performed with caution. CONCLUSION A brief, intense exercise regimen designed to improve distal lower extremity strength was well tolerated and improved 3 clinical parameters of balance in a group of older persons with PN. Although increased confidence or distal lower extremity strength may be responsible for these findings, the study provided no clear insight into the mechanism of the improvements seen in the intervention group. Whether the improvements in clinical balance noted in the intervention subjects translate into decreased fall risk in daily life is unknown. However, given the minimal risk from the intervention exercises and the magnitude of the benefit from preventing falls in the population studied, it appears reasonable for clinicians to consider prescribing these exercises for their patients with postural instability caused by PN. Arch Phys Med Rehabil Vol 82, February 2001
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